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Journal of Chemical Ecology

, Volume 34, Issue 12, pp 1518–1522 | Cite as

Pathogen-induced Release of Plant Allomone Manipulates Vector Insect Behavior

  • Christoph J. Mayer
  • Andreas Vilcinskas
  • Jürgen Gross
Article

Abstract

Infochemicals mediate communication within and between different trophic levels. In this study, we identified a new type of plant allomone induced by a plant pathogen and perceived by its vector insect Cacopsylla picta. This phloem-feeding psyllid is the main vector of Candidatus Phytoplasma mali, a cell wall-lacking bacterium that causes the so-called apple proliferation disease. In a previous study, we showed that newly emerged females of C. picta were attracted by the odor of phytoplasma-infected apple plants (Malus domestica), which release ß-caryophyllene in contrast to uninfected plants. Here, the attractiveness of this sesquiterpene for C. picta was confirmed in both olfactometer bioassays and field studies. Synthetic ß-caryophyllene was highly attractive to newly emerged adults of C. picta both when offered simultaneously with healthy apple odor and without. The psyllid’s response was independent of its odor experience and infection status. These results confirm our previously established hypothesis that this phytoplasma manipulates the behavior of its vector insect by changing the odor blend of its host plant. Deployed in apple orchards, sticky traps baited with ß-caryophyllene dispensers caught both males and females of C. picta. Consequently, this new type of infochemical, i.e., a phytopathogen-induced plant allomone, represents a promising compound to develop innovative techniques for monitoring or maybe even mass trapping of C. picta.

Keywords

Apple proliferation Vector–plant–pathogen interaction ß-caryophyllene Candidatus Phytoplasma mali Cacopsylla picta Malus domestica 

Notes

Acknowledgements

This work was funded by the German Research Foundation (DFG GR 2645/1,2). J.G. is grateful to the Stifterverband für die Deutsche Wissenschaft for additional funding (innovative research award). We thank Jürgen Just and Kai Lukat for excellent technical assistance and Eva Gross for linguistic improvements.

References

  1. Dicke, M., and Sabelis, M. W. 1988. Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? Funct. Ecol. 2:131–139.CrossRefGoogle Scholar
  2. Frisinghelli, C., Delaiti, L., Grando, M. S., Forti, D., and Vindimian, M. E. 2000. Cacopsylla costalis (Flor 1861), as a vector of apple proliferation in Trentino. J. Phytopathol. 148:425–431.CrossRefGoogle Scholar
  3. Khalilova, A. Z., Paramonov, E. A., Odinokov, V. N., and Khalilov, L. M. 1998. Identification and biological activity of volatile organic substances emitted by plants and insects. 1. Components of the native scents of Leptinotarsa decemlineata and Solanum tuberosum. Chem. Nat. Comp. 34:647–649.CrossRefGoogle Scholar
  4. Mayer, C. J., Vilcinskas, A., and Gross, J. 2008a. Phytopathogen lures its insect vector by altering host plant odor. J. Chem. Ecol. 34:1045–1049.PubMedCrossRefGoogle Scholar
  5. Mayer, C. J., Jarausch, B., Jarausch, W., Vilcinskas, A., and Gross, J. 2008b. Cacopsylla melanoneura has no relevance as vector of apple proliferation in Germany. Phytopathology (in press)Google Scholar
  6. Mumm, R., Posthumus, M. A., and Dicke, M. 2008. Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ. 31:575–585.PubMedCrossRefGoogle Scholar
  7. Rasmann, S., Köllner, T. G., Degenhard, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J., and Turlings, T. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737.PubMedCrossRefGoogle Scholar
  8. Rostás, M., Simon, M., and Hilker , M. 2003. Ecological cross effects of induced plant responses towards herbivores and phytopathogenic fungi. Basic Appl. Ecol. 4:43–62.CrossRefGoogle Scholar
  9. Schnee, C., Kollner, T. G., Held, M., Turlings, T. C. J., Gershenzon, J., and Degenhardt, J. 2006. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Natl. Acad. Sci. USA 103:1129–1134.PubMedCrossRefGoogle Scholar
  10. Seemüller, E., and Schneider, B. 2004. ‘Candidatus Phytoplasma mali’, ‘Candidatus Phytoplasma pyri’ and ‘Candidatus Phytoplasma prunorum’, the causal agents of apple proliferation, pear decline and European stone fruit yellows, respectively. Int. J. Syst. Evol. Microbiol. 53:1217–1226.CrossRefGoogle Scholar
  11. Seemüller, E., Garnier, M., and Schneider, B. 2002. Mycoplasmas of plants and insects, pp. 91–116, in S. Razin, and R. Herrmann (eds.). Molecular Biology and Pathology of Mycoplasmas. Kluwer Acad. Publ., London.CrossRefGoogle Scholar
  12. Stout, M. J., Thaler, J. S., and Thomma, B. P. H. J. 2006. Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu. Rev. Entomol. 51:663–689.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Christoph J. Mayer
    • 1
    • 2
  • Andreas Vilcinskas
    • 1
  • Jürgen Gross
    • 1
    • 2
  1. 1.Institute for Phytopathology and Applied ZoologyJustus-Liebig UniversityGießenGermany
  2. 2.Julius Kuehn Institute—Federal Research Centre for Cultivated PlantsInstitute for Plant Protection in Fruit Crops and ViticultureDossenheimGermany

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